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Effects of plant growth-promoting rhizobacteria on nodulation of Phaseolus vulgaris L. are dependent on plant P nutrition

  • Roseline RemansEmail author
  • Anja Croonenborghs
  • Roldan Torres Gutierrez
  • Jan Michiels
  • Jos Vanderleyden
Chapter

Abstract

Several plant growth-promoting rhizobacteria (PGPR) have shown potential to enhance nodulation of legumes when coinoculated with Rhizobium. To optimize the efficiency of these Rhizobium-PGPR-host plant interactions, unravelling the underlying mechanisms and analyzing the influence of specific environmental conditions is crucial. In this work the effect of four PGPR strains on the symbiotic interaction between Rhizobium and common bean (Phaseolus vulgaris) was studied under deficient versus sufficient phosphorus supply. It was observed that the effect on nodulation of three out of four PGPR tested was strongly dependent on P nutrition. Further, the use of specific PGPR mutant strains indicated that bacterial indole-3-acetic-acid production (IAA) and l-aminocyclopropane-l-carboxylate (ACC) deaminase activity play an important role in the host nodulation response, particularly under low P conditions. Moreover, it was shown that the differential response to PGPR under low versus high P conditions was associated with changes in the host hormone sensitivity for nodulation induced under P deficiency. These findings contribute to the understanding of the interplay between Rhizobium, PGPR and the plant host under different environmental settings.

Keywords

Phosphorus deficiency Nodulation Common bean Plant growth-promoting rhizobacteria Phytohormones 

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References

  1. Al-Ghazi, Y., Muller, B., Pinloche, S., Tranbarger, T. J., Rossignol, M., Tardieu, F., & Doumas, P. (2003). Temporal responses of Arabidopsis root architecture to phosphate starvation: Evidence for the involvement of auxin signaling. Plant, Cell and Environment, 26, 1053–1066.CrossRefGoogle Scholar
  2. AI-Niemi, T. S., Kahn, M. L., & McDermott, T. R. (1997). P metabolism in the bean-Rhizobium-tropici symbiosis. Plant Physiology, 113, 1233–1242.Google Scholar
  3. Bai, Y., Panb, B., Charlesc, T., & Smith, D. (2002). Co-inoculation dose and root zone temperature for plant growth promoting rhizobacteria on soybean [Glycine max (L.) Merr] grown in soil-less media. Soil Biology and Biochemistry, 34, 1953–1957.CrossRefGoogle Scholar
  4. Bai, Y., Zhou, X., & Smith, D. (2003). Enhanced soybean plant growth resulting from coinoculation of Bacillus strains with Bradyrhizobium japonicum. Crop Science, 43, 1174–1781.Google Scholar
  5. Baldani, V. L. D., Alvarez, M. A. B., Baldani, J. I., & Döbereiner, J. (1986). Establishment of inoculated Azospirillum spp. in the rhizosphere and in roots of field grown wheat and sorghum. Plant Soil, 90, 37–40.CrossRefGoogle Scholar
  6. Bolton, H., Elliott, L. F., Turco, R. F., & Kennedy, A. C. (1990). Rhizoplane colonization of pea seedlings by Rhizobium leguminosarum and a deleterious root colonizing Pseudomonas sp. and effects on plant growth. Plant Soil, 123, 121–124.Google Scholar
  7. Borch, K., Bouma, T. J., Lynch, J. P., & Brown, K. M. (1999). Ethylene: A regulator of root architectural responses to soil phosphorus availability. Plant Cell Environment, 22, 425–431.CrossRefGoogle Scholar
  8. Broughton, W. J., Hernander, G., Blair, B., Beebe, S., Gepts, P., & Vanderleyden, J. (2003). Beans (Phaseolus spp.) — model food legumes. Plant Soil, 252, 55–128.CrossRefGoogle Scholar
  9. Burdman, S., Kigel, J., & Okon, Y. (1997). Effects of Azospirillum brasilense on nodulation and growth of common bean (Phaseolus vulgaris L.). Soil Biology and Biochemistry, 29, 923–929.CrossRefGoogle Scholar
  10. Burdman, S., Volpin, H., Kigel, J., Kapulnik, Y., & Okon, Y. (1996). Promotion of nod gene inducers and nodulation in common bean (Phaseolus vulgaris) roots inoculated with Azospirillum brasilense Cd. Applied and Environmental Microbiology, 62, 3030–3033.PubMedGoogle Scholar
  11. Bums, T. A., Bishop, P. E., & Israel, D. W. (1981). Enhanced nodulation of leguminous plant roots by mixed cultures of Azotobacter vinelandi and damping-off of tomato by Pseudomonas aeruginosa 7NSK2. Applied and Environmental Microbiology, 62, 865–871.Google Scholar
  12. Camacho, M., Santamaria, C., Temprano, F., RodriguezNavarro, D. N., & Daza, A. (2001). Co-inoculation with Bacillus sp. CECT 450 improves nodulation in Phaseolus vulgaris L. Canadian Journal of Microbiology, 47, 1058–1062.CrossRefPubMedGoogle Scholar
  13. Christiansen, I., & Graham, P. H. (2002). Variation in dinitrogen fixation among Andean bean (Phaseolus vulgaris L.) genotypes grown at low and high levels of phosphorus supply. Fields Crops Research, 73, 133–142.CrossRefGoogle Scholar
  14. Chun, J., & Bae, K. S. (2000). Phylogenetic analysis of Bacillus subtilis and related taxa based on partial gyrA gene sequences. Antonie Leeuwenhoek, 78, 123–127.CrossRefPubMedGoogle Scholar
  15. Costacurta, A., Keijers, V., & Vanderleyden, J. (1994). Molecular cloning and sequence analysis of an Azospirillum brasilense indole-3-pyruvate decarboxylase gene. Molecular and General Genetics, 243, 463–472.PubMedGoogle Scholar
  16. Dashti, N., Zhang, F., Hynes, R., & Smith, D. L. (1998). Plant growth promoting rhizobacteria accelerate nodulation and increase nitrogen fixation activity by field grown soybean [Glycine max (L.) Merr.] under short season conditions. Plant Soil, 200, 205–213.CrossRefGoogle Scholar
  17. Dobbelaere, S., Croonenborghs, A., Thys, A., Vande Broek, A., & Vanderleyden, J. (1999). Phytostimulatory effect of Azospiriilum brasilense wild type and mutant strains altered in IAA production on wheat. Plant Soil, 212, 155–164.CrossRefGoogle Scholar
  18. Franzluebbers, K., Hossner, L. R., & Juo, A. S. R. (1998). Integrated nutrient management for sustained crop production in sub-Saharan agriculture. Trop Soils/TAMU Technical Bulletin No. 98-03, 50 pp.Google Scholar
  19. Glick, B. R., Karaturovíc, D. M., & Newell, P. C. (1995). A novel procedure for rapid isolation of plant growthpromoting pseudomonads. Canadian Journal of Microbiology, 41, 533–536.CrossRefGoogle Scholar
  20. Goel, A. K., Sindhu, S. S., & Dadarwal, K. R. (2002). Stimulation of nodulation and plant growth of chickpea (Cicer arietnum L.) by Pseudomonas spp. antagonistic to fungal pathogens. Biology and Fertility of Soils, 36, 391–396.CrossRefGoogle Scholar
  21. Graham, P. H. (1981). Some problems of nodulation and symbiotic nitrogen fixation in Phaseolus vulgaris L.: A review. Field Crops Research, 4, 93–112.CrossRefGoogle Scholar
  22. Graham, P. H., & Rosas, J. C. (1979). Phosphorus fertilization and symbiotic nitrogen fixation in common bean. Agronomy Journal, 71, 925–926.Google Scholar
  23. Hamaoui, B., Abbadi, J. M., Burdman, S., Rashid, A., Sarig, S., & Okon, Y. (2001). Effects on inoculation with Azospirillum brasilense on chickpeas (Cicer arietum) and faba beans (Vicia faba) under different growth conditions. Agronomie, 21, 553–560.CrossRefGoogle Scholar
  24. Hontzeas, N., Saleh, S. S., & Glick, B. R. (2004). Changes in gene expression in canola roots induced by ACC-deaminase-containing plant-growth-promoting bacteria. Molecular Plant Microbe Interactions, 17, 865–871.CrossRefPubMedGoogle Scholar
  25. Kouas, S., Labidi, N., Debez, A., & Abdelly, C. (2005). Effect of P on nodule formation and N fixation in bean. Agronomy for Sustainable Development, 25, 389–393.CrossRefGoogle Scholar
  26. Li, J., Ovakim, D. H., Charles, T. C., & Glick, B. R. (2000). An ACC deaminase minus mutant of Enterobacter cloacae UW4 no longer promotes root elongation. Current Microbiology, 41, 101–105.CrossRefPubMedGoogle Scholar
  27. Lopez-Bucio, J., Hernandez-Abreu, E., Sanchez-Calderon, L., Nieto-Jacobo, M. F., Simpson, J., & Herrera-Estrella, L. (2002). Phosphate availability alters architecture and causes changes in hormone sensitivity in the Arabidopsis root system. Plant Physiology, 129, 244–256.CrossRefPubMedGoogle Scholar
  28. Lugtenberg, B. J. J., Chin-A-Woeng, T. F. C., & Bloemberg, G. V. (2002). Microbe-plant interactions: Principles and mechanisms. Antonie Leeuwenhoek, 81, 373–383.CrossRefPubMedGoogle Scholar
  29. Ma, W., Charles, T. C., & Glick, B. R. (2004). Expression of an exogenous l-aminocyclopropane-l-carboxylate deaminase gene in Sinorhizobium meliloti increases its ability to nodulate alfalfa. Environmental Microbiology, 70, 5891–5897.CrossRefGoogle Scholar
  30. Michiels, J., Moris, M., Dombrecht, B., Verreth, C., & Vanderleyden, J. (1998). Differential regulation of Rhizobium etli rpoN2 gene expression during symbiosis and free-living growth. Journal of Bacteriology, 180, 3620–3628.PubMedGoogle Scholar
  31. Oldroyd, G. E., Engstrom, E. M., & Long, S. R. (2001). Ethylene inhibits the Nod factor signal transduction pathway of Medicago truncatula. Plant Cell, 13, 1835–1849.CrossRefPubMedGoogle Scholar
  32. Ona, O., Van Impe, J., Prinsen, E., & Vanderleyden, J. (2005). Growth and indole-3-acetic acid biosynthesis of Azospirillum brasilense Sp245 is environmentally controlled. FEMS Microbiology Letters, 246, 125–132.CrossRefPubMedGoogle Scholar
  33. Penmetsa, R. V., & Cook, D. R. (1997). A legume ethyleneinsensitive mutant hyperinfected by its rhizobial symbiont. Science, 257, 527–530.CrossRefGoogle Scholar
  34. Pepper, J. L. (2000). Beneficial and pathogenic microbes in agriculture. In R. M. Maier et al. (Eds.), Environmental microbiology. San Diego: Academic Press.Google Scholar
  35. Pereira, P. A., & Bliss, F. A. (1987). Nitrogen fixation and plant growth of common bean (Phaseolus vulgaris L.) at different levels of phosphorus availability. Plant Soil, 104, 79–84.CrossRefGoogle Scholar
  36. Persello-Cartieaux, F., Nussaume, L., & Robaglia, C. (2003). Tales from the underground: Molecular plant-rhizobacteria interactions. Plant, Cell and Environment, 26, 189–199.CrossRefGoogle Scholar
  37. Plazinski, J., & Rolfe B. G. (1985a). Azospirillum-Rhizobium interaction leading to a plant growth stimulation without nodule formation. Canadian Journal of Microbiology, 31, 1026–1030.CrossRefGoogle Scholar
  38. Plazinski, J., & Rolfe, B. G. (1985b). Interaction of Azospirillum and Rhizobium strains leading to inhibition of nodulation. Applied and Environmental Microbiology, 49, 990–993.PubMedGoogle Scholar
  39. Plazinski, J., & Rolfe, B. G. (1985c). Influence of Azospirillum strains on the nodulation of clovers by Rhizobium strains. Applied and Environmental Microbiology, 49, 984–989.PubMedGoogle Scholar
  40. Rainey, P. B., & Bailey, M. J. (1996). Physical map of the Pseudomonas fiuorescens SBW25 chromosome. Molecular Microbiology, 19, 521–533.CrossRefPubMedGoogle Scholar
  41. Raverker, K. P., & Konde, B. K. (1988). Effect of Rhizobium and Azospirillum lipoferum inoculation on nodulation, yield and nitrogen uptake of peanut cultivars. Plant Soil, 106, 249–252.CrossRefGoogle Scholar
  42. Sambrook, J., Fritsch, E. F., & Maniatis, T. (1989). Molecular cloning: A laboratory manual (2nd ed.). Cold Spring Harbor, N.Y.: Cold Spring Harbor Laboratory Press.Google Scholar
  43. SAS Institute (1996). SAS user’s guide: Statistics (6th ed.). Cary, NC: SAS Institute.Google Scholar
  44. Schulze, J., Temple, G., Temple, S. J., Beschow, H., & Vance, C. P. (2006). Nitrogen fixation by white lupin under phosphorus deficiency. Annals of Botany, 98, 731–740.CrossRefPubMedGoogle Scholar
  45. Sindhu, S. S., Gupta, S. K., & Dadarwal, K. R. (1999). Antagonistic effect of Pseudomonas spp. on pathogenic fungi and enhancement of plant growth in green gram (Vigna radiata). Biology and Fertility of Soils, 29, 62–68.CrossRefGoogle Scholar
  46. Smith, D. L., & Hume, D. J. (1987). Comparison of assay methods for nitrogen fixation utilizing white bean and soybean. Canadian Journal of Plant Science, 67, 11–79.CrossRefGoogle Scholar
  47. Snoeck, C., Verreth, C., Hernandez-Lucas, I., MartinezRomero, E., & Vanderleyden, J. (2003). Identification of a third sulfate activation system in Sinorhizobium sp. strain BR816: The CysDN sulfate activation complex. Applied and Environmental Microbiology, 69, 2006–2014.CrossRefPubMedGoogle Scholar
  48. Srinivasan, M., Petersen, D. J., & Holl, F. B. (1997). Influence of indoleacetic-acid-producing Bacillus isolates on the nodulation of Phaseolus vulgaris by Rhizobium etli under gnobiotic conditions. Canadian Journal of Microbiology, 42, 1006–1014.CrossRefGoogle Scholar
  49. Tchebotar, V. K., Kang, U. G., Asis, C. A., & Akao, J. S. (1998). The use of GUS-reporter gene to study the effect of Azospirillum-Rhirobium coinoculation on nodulation of white clover. Biology and Fertility of Soils, 27, 349–352.CrossRefGoogle Scholar
  50. Thilak, K. V. B. R., Ranganayaki, N., & Manoharachari, C. (2006). Synergistic effects of plant-growth promoting rhizobacteria and Rhizobium on nodulation and nitrogen fixation by pigeonpea (Cajanus cajan). European Journal of Soil Science, 57, 67–71.CrossRefGoogle Scholar
  51. Thung, M. (1991). Bean agronomy in monoculture. In A. V. Schoonhoven & O. Voysest (Eds.), Common beans. Research for crop improvement (pp. 737–834). Wallingford, UK: CAB International.Google Scholar
  52. Vadez, V., Lasso, J. H., Beck, D. P., & Drevon, J. J. (1999). Variability of N2-fixation in common bean (Phaseolus vulgaris L.) under P deficiency is related to P use efficiency. Euphytica, 106, 231–242.CrossRefGoogle Scholar
  53. Vance, C. P. (1997). Enhanced agricultural sustainability through biological nitrogen fixation. In A. Legocki et al. (Eds.), Biological fixation of nitrogen for ecology and sustainable agriculture. Heidelberg, Germany: NATO ASI Series, Springer-Verslag.Google Scholar
  54. Vance, C. P., Graham, P. H., & Allan, D. L. (2000). Biological nitrogen fixation: Phosphorus-a critical need. In F. A. Pedrosa et al. (Eds.), Nitrogen fixation: From molecules to crop productivity (pp. 509–514). Netherlands: Kluwer Academic Publishers.Google Scholar
  55. Vande Broek, A., Lambrecht, M., Eggermont, K., & Vanderleyden, J. (1999). Auxins upregulate expression of the indole-3-pyruvate decarboxylase gene in Azospirillum brasilense. Journal of Bacteriology, 181, 1338–1342.Google Scholar
  56. Van Noorden, G. E., Ross, J. J., Reid, J. B., Rolfe, B. G., & Mathesius, U. (2006). Defective long distance auxin transport regulation in the Medicago truncatula super numeric nodules mutant. Plant Physiology, 140, 1494–1506.CrossRefPubMedGoogle Scholar
  57. Vessey, K., & Buss, T. J. (2002). Bacillus cereus UW85 inoculation effects on growth, nodulation, and N accumulation in grain legumes — Controlled-environment studies. Canadian Journal of Plant Science, 82, 282–290.Google Scholar
  58. Vincent, J. M. (1970). A manualfor the practical study of rootnodule bacteria. Oxford: Blackwell Scientific Publishers.Google Scholar
  59. Vlassak, K. M., Luyten, E., Verreth, C., van Rhijn, P., Bisseling, T., & Vanderleyden, J. (1998). The Rhizobium sp. BR816 nodO gene can function as a determinant for nodulation of Leucaena leucocephala, Phaseolus vulgaris and Trifolium repens by a diversity of Rhizobium spp. Molecular Plant Microbe Interactions, 5, 383–392.CrossRefGoogle Scholar
  60. Volpin, H., Burdman, S., Castro-Sowinski, S., Kapulnik, Y., & Okon, Y. (1996). Inoculation with Azospirillum increased exudation of Rhizobial nod-gene inducers by alfalfa roots. Molecular Plant Microbe Interactions, 1996, 388–394.Google Scholar
  61. Woodward, A. W., & Bartel, B. (2005). Auxin: Regulation, action and interaction. Annals of Botany, 95, 707–735.CrossRefPubMedGoogle Scholar
  62. Xie, H., Pasternak, J. J., & Glick, B. R. (1996). Isolation and characterization of mutants of the plant growth-promoting rhizobacterium Pseudomonas putida CR12-2 that overproduce indoleacetic acid. Current Microbiology, 32, 67–71.CrossRefGoogle Scholar

Copyright information

© KNPV 2007

Authors and Affiliations

  • Roseline Remans
    • 1
    Email author
  • Anja Croonenborghs
    • 1
  • Roldan Torres Gutierrez
    • 1
  • Jan Michiels
    • 1
  • Jos Vanderleyden
    • 1
  1. 1.Department of Microbial and Molecular Systems, Centre of Microbial and Plant GeneticsK.U. LeuvenHeverleeBelgium

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